Messenger RNA Sequencing and Pathway Analysis Provide Novel Insights Into the Susceptibility to Salmonella enteritidis Infection in Chickens

Salmonella enteritidis (SE) is a foodborne pathogen that negatively affects both animal and human health. Controlling poultry SE infection will have great practical significance for human public health, as poultry are considered to be important sources and carriers of the disease. In this study, the...

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Main Authors: Peng Li, Wenlei Fan, Nadia Everaert, Ranran Liu, Qinghe Li, Maiqing Zheng, Huanxian Cui, Guiping Zhao, Jie Wen
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-07-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2018.00256/full
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author Peng Li
Peng Li
Peng Li
Wenlei Fan
Wenlei Fan
Nadia Everaert
Ranran Liu
Qinghe Li
Maiqing Zheng
Huanxian Cui
Guiping Zhao
Jie Wen
Jie Wen
author_facet Peng Li
Peng Li
Peng Li
Wenlei Fan
Wenlei Fan
Nadia Everaert
Ranran Liu
Qinghe Li
Maiqing Zheng
Huanxian Cui
Guiping Zhao
Jie Wen
Jie Wen
author_sort Peng Li
collection DOAJ
description Salmonella enteritidis (SE) is a foodborne pathogen that negatively affects both animal and human health. Controlling poultry SE infection will have great practical significance for human public health, as poultry are considered to be important sources and carriers of the disease. In this study, the splenic transcriptomes of challenged-susceptible (S), challenged-resistant (R) and non-challenged (C) chicks (3-days old, specific-pathogen-free White Leghorn) were characterized in order to identify the immune-related gene markers and pathways. A total of 934 significant differentially expressed genes (DEGs) were identified in comparisons among the C, R and S birds. First reported here, the DEGs involved in the Forkhead box O (FoxO) signaling pathway, especially FoxO3, were identified as potential markers for host resistance to SE infection. The challenged-susceptible birds exhibited strong activation of the FoxO signaling pathway, which may be a major defect causing immune cell apoptosis as part of SE-induced pathology; these S birds also showed weak activation of mitogen-activated protein kinase (MAPK)-related genes, contrasting with strong splenic activation in the R birds. Interestingly, suppression of several pathways in the immune response against Salmonella, including cytokine-cytokine receptor interaction and Jak-STAT, was only found in S birds and there was evidence of cross-talk among these pathways, perhaps contributing to susceptibility to Salmonella infection. These findings will help facilitate understanding resistance and susceptibility to SE infection in the earliest phases of the host immune response through Salmonella-induced pathways, provide new approaches to develop strategies for SE prevention and treatment, and may enhance innate resistance by genetic selection in animals.
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spelling doaj.art-41bfd5b2c0cc4a6ca631e1a67e1fa4da2022-12-21T17:13:19ZengFrontiers Media S.A.Frontiers in Genetics1664-80212018-07-01910.3389/fgene.2018.00256365476Messenger RNA Sequencing and Pathway Analysis Provide Novel Insights Into the Susceptibility to Salmonella enteritidis Infection in ChickensPeng Li0Peng Li1Peng Li2Wenlei Fan3Wenlei Fan4Nadia Everaert5Ranran Liu6Qinghe Li7Maiqing Zheng8Huanxian Cui9Guiping Zhao10Jie Wen11Jie Wen12Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, ChinaPrecision Livestock and Nutrition Unit, Gembloux Agro-Bio Tech, TERRA Teaching and Research Centre, University of Liège, Gembloux, BelgiumState Key Laboratory of Animal Nutrition, Beijing, ChinaInstitute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory of Animal Nutrition, Beijing, ChinaPrecision Livestock and Nutrition Unit, Gembloux Agro-Bio Tech, TERRA Teaching and Research Centre, University of Liège, Gembloux, BelgiumInstitute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, ChinaInstitute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, ChinaInstitute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, ChinaInstitute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, ChinaInstitute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, ChinaInstitute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, ChinaState Key Laboratory of Animal Nutrition, Beijing, ChinaSalmonella enteritidis (SE) is a foodborne pathogen that negatively affects both animal and human health. Controlling poultry SE infection will have great practical significance for human public health, as poultry are considered to be important sources and carriers of the disease. In this study, the splenic transcriptomes of challenged-susceptible (S), challenged-resistant (R) and non-challenged (C) chicks (3-days old, specific-pathogen-free White Leghorn) were characterized in order to identify the immune-related gene markers and pathways. A total of 934 significant differentially expressed genes (DEGs) were identified in comparisons among the C, R and S birds. First reported here, the DEGs involved in the Forkhead box O (FoxO) signaling pathway, especially FoxO3, were identified as potential markers for host resistance to SE infection. The challenged-susceptible birds exhibited strong activation of the FoxO signaling pathway, which may be a major defect causing immune cell apoptosis as part of SE-induced pathology; these S birds also showed weak activation of mitogen-activated protein kinase (MAPK)-related genes, contrasting with strong splenic activation in the R birds. Interestingly, suppression of several pathways in the immune response against Salmonella, including cytokine-cytokine receptor interaction and Jak-STAT, was only found in S birds and there was evidence of cross-talk among these pathways, perhaps contributing to susceptibility to Salmonella infection. These findings will help facilitate understanding resistance and susceptibility to SE infection in the earliest phases of the host immune response through Salmonella-induced pathways, provide new approaches to develop strategies for SE prevention and treatment, and may enhance innate resistance by genetic selection in animals.https://www.frontiersin.org/article/10.3389/fgene.2018.00256/fullspleen transcriptomeSalmonella enteritidisresistant and susceptibleimmune-related genes and pathwaychicken
spellingShingle Peng Li
Peng Li
Peng Li
Wenlei Fan
Wenlei Fan
Nadia Everaert
Ranran Liu
Qinghe Li
Maiqing Zheng
Huanxian Cui
Guiping Zhao
Jie Wen
Jie Wen
Messenger RNA Sequencing and Pathway Analysis Provide Novel Insights Into the Susceptibility to Salmonella enteritidis Infection in Chickens
Frontiers in Genetics
spleen transcriptome
Salmonella enteritidis
resistant and susceptible
immune-related genes and pathway
chicken
title Messenger RNA Sequencing and Pathway Analysis Provide Novel Insights Into the Susceptibility to Salmonella enteritidis Infection in Chickens
title_full Messenger RNA Sequencing and Pathway Analysis Provide Novel Insights Into the Susceptibility to Salmonella enteritidis Infection in Chickens
title_fullStr Messenger RNA Sequencing and Pathway Analysis Provide Novel Insights Into the Susceptibility to Salmonella enteritidis Infection in Chickens
title_full_unstemmed Messenger RNA Sequencing and Pathway Analysis Provide Novel Insights Into the Susceptibility to Salmonella enteritidis Infection in Chickens
title_short Messenger RNA Sequencing and Pathway Analysis Provide Novel Insights Into the Susceptibility to Salmonella enteritidis Infection in Chickens
title_sort messenger rna sequencing and pathway analysis provide novel insights into the susceptibility to salmonella enteritidis infection in chickens
topic spleen transcriptome
Salmonella enteritidis
resistant and susceptible
immune-related genes and pathway
chicken
url https://www.frontiersin.org/article/10.3389/fgene.2018.00256/full
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